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Persoff has amassed a career consisting of well over 200 film and television appearances. Early in his career, he became well-known for playing villainous, tough guy roles such as mobsters and gangsters, such as those in the classic films The Wrong Man, Al Capone, and Some Like It Hot. Most notably, he had a recurring role as gangster Jake 'Greasy Thumb' Guzik on the Desilu series The Untouchables.

Since then, however, Persoff has become known for playing kinder, gentler roles. His most notable of such roles were a pair of "Papa" characters in two different films from the 1980s: Rabi Reb Mendel, Yentl's father, in the 1983 musical drama Yentl; and Papa Mouskewitz in the 1986 animated film An American Tail and its sequels.

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Persoff was born in Jerusalem, Palestine (now Israel) and emigrated to America with his family in 1929. He won a scholarship to the Dramatic Workshop in New York, which led to his New York stage debut in a 1940 production of The Emperor's New Clothes. A veteran of World War II, Persoff served in the United States Army from 1942 to 1946 before being discharged as a Technician 5th Grade.

Following his military service, Persoff returned to his acting career, making his Broadway debut in Galileo in December 1947. Warren Stevens also performed in this production. The following year, Persoff appeared in his second Broadway play, Sundown Beach, again working with Warren Stevens.

In 1954, Persoff worked with William Windom in the play Mademoiselle Colombe. Later that year, he acted with Georgann Johnson and David Opatoshu in Reclining Figure. Persoff was then part of the original cast of the Tony Award-nominated play Tiger at the Gates in 1956. His last Broadway production was Only in America in 1959.

Persoff made his film debut in the 1948 noir classic The Naked City. His second film role was the obscure cab driver during Marlon Brando's classic "I coulda been a contender" scene in 1954's On the Waterfront. Persoff made his first credited film appearance in 1956's The Harder They Fall.

He acted alongside Jay Robinson in the 1956 crime drama The Wild Party. That same year, Persoff was seen in Alfred Hitchcock's noir classic The Wrong Man, along with Charles Cooper. Persoff then co-starred with Phillip Pine and Scott Marlowe in the 1957 drama Men in War. In 1958's The Badlanders, Pursoff worked with Anthony Caruso.

Persoff played a mobster Johnny Torrio in the 1959 biopic Al Capone, which also starred James Gregory. Later that year, Persoff and Elisha Cook, Jr., appeared in the western Day of the Outlaw. In addition, Persoff played a gangster in the acclaimed 1959 comedy Some Like It Hot.

He co-starred in the 1961 western adventure The Comancheros, along with veteran Trek guest star Michael Ansara had a role in this film. Persoff and Ansara were also a part of the extensive ensemble cast of the 1965 biblical epic The Greatest Story Ever Told, as was Mark Lenard.

Persoff has made over two hundred television guest appearances since 1949. His most famous TV role is that of mobster Jake "Greasy Thumb" Guzik in three episodes of the popular CBS series The Untouchables, which, like Star Trek, was produced by Desilu. He made his first appearance as Guzik in 1959 and reprised the role in 1961 (in an episode with Joseph Ruskin) and 1962 (in an episode with Barry Russo and Malachi Throne). Persoff appeared in three other episodes of The Untouchables, playing a different character in each. One episode co-starred Madlyn Rhue; another co-starred Michael Strong.

Persoff has also guest-starred in multiple episodes of Gunsmoke (including one directed by Vincent McEveety, one with Anthony Zerbe, one with Robert DoQui), three episodes of The Wild Wild West (including one with Al Capone co-star James Gregory and another with Jeff Corey and Sabrina Scharf) and three episodes of Mission: Impossible. In his first episode of Mission: Impossible, "Odds of Evil," Persoff played a prince while Lawrence Montaigne played his aide. In his third episode, "Fool's Gold," Persoff worked with David Opatoshu. At that point, Star Trek: The Original Series star Leonard Nimoy was a regular on Mission: Impossible; Persoff previously worked with Nimoy on the western series Wagon Train.

Herschel Daugherty directed Persoff in a 1960 episode of Alfred Hitchock Presents and in a 1969 episode of Hawaii Five-O, a series Persoff returned to many times in the 1970s. In 1964, Persoff appeared with Jane Wyatt on Bob Hope Presents the Chrysler Theatre. The following year, Persoff guest-starred on For the People, the series William Shatner starred in before he joined Star Trek.

Although he was known for "tough guy" roles during the 1950s and 1960s, Persoff has more recently become known for more light-hearted characters. His best-known film role is that of Yentl's "Papa" in the 1983 musical drama Yentl. He is also known for voicing Papa Mousekewitz in the 1986 animated film An American Tail, its 1991 sequel An American Tail: Fievel Goes West (in which Phillip Glasser played Papa's son, Fievel), and two direct-to-video sequels in which Thomas Dekker voiced Fievel. Christopher Plummer voiced Henri the pigeon in the first American Tail, while Rene Auberjonois, Tony Jay, John Kassir, and Ron Perlman voiced characters in the 1998 video sequel An American Tail: The Treasure of Manhattan Island.

Due to declining health and high blood pressure, Persoff was forced to limit his acting work in the mid-1980s. To compensate for his decreased acting workload, Persoff took up painting as a hobby in 1985. He did continue making occasional film and television appearances, however. He appeared as a Rabbi in Martin Scorsese's acclaimed, controversial film The Last Temptation of Christ and played a supporting role in the hit 1988 comedy film Twins. The latter project also featured the aforementioned Tony Jay as well as Robert Harper, Tom McCleister, Dendrie Taylor, and Cary-Hiroyuki Tagawa.

In addition, Persoff made guest appearances on such television series as Magnum, P.I. (in an episode with France Nuyen and directed by Leo Penn), L.A. Law (starring Corbin Bernsen and Larry Drake, in an episode directed by David Carson and co-starring Diana Muldaur and Natalia Nogulich), Murder, She Wrote (with James Sloyan), Doogie Howser, M.D. (on which Lawrence Pressman and James B. Sikking were regulars), and Law & Order. Persoff has since retired from acting entirely, instead devoting himself to his painting. Specializing in watercolor, he has created many works of art, many of which have been exhibited in California.